Plicidentine and the repeated origins of snake venom fangs.

Alessandro Palci,Silke G C Cleuren,Michael W Caldwell,Hyab Mehari Abraha,Mark N Hutchinson,Michael S Y Lee,Aaron R H Leblanc,Alistair R Evans,Olga Panagiotopoulou

doi:10.1098/rspb.2021.1391

Abstract

Snake fangs are an iconic exemplar of a complex adaptation, but despite striking developmental and morphological similarities, they probably evolved independently in several lineages of venomous snakes. How snakes could, uniquely among vertebrates, repeatedly evolve their complex venom delivery apparatus is an intriguing question. Here we shed light on the repeated evolution of snake venom fangs using histology, high-resolution computed tomography (microCT) and biomechanical modelling. Our examination of venomous and non-venomous species reveals that most snakes have dentine infoldings at the bases of their teeth, known as plicidentine, and that in venomous species, one of these infoldings was repurposed to form a longitudinal groove for venom delivery. Like plicidentine, venom grooves originate from infoldings of the developing dental epithelium prior to the formation of the tooth hard tissues. Derivation of the venom groove from a large plicidentine fold that develops early in tooth ontogeny reveals how snake venom fangs could originate repeatedly through the co-option of a pre-existing dental feature even without close association to a venom duct. We also show that, contrary to previous assumptions, dentine infoldings do not improve compression or bending resistance of snake teeth during biting; plicidentine may instead have a role in tooth attachment.

Highlights

Snakes are unparalleled among vertebrates in their evolution of sophisticated venom delivery systems, which consist of venom glands, highly modified teeth for venom injection and associated muscles and bones [1,2,3]
We investigated tooth microstructure across the major snake clades using multiple approaches, in order to (i) verify whether plicidentine is present in snakes; (ii) determine if plicidentine is developmentally correlated with the origin of venom grooves and (iii) formulate a novel hypothesis of snake fang origin and evolution based on the examination of tooth microanatomy, development, and biomechanics
To test the mechanical function of the plicidentine and venom groove during biting, we created a series of models where plicidentine infoldings and/or the venom groove were removed while keeping the total dentine volume approximately constant

Summary

Introduction

Snakes are unparalleled among vertebrates in their evolution of sophisticated venom delivery systems, which consist of venom glands, highly modified teeth for venom injection and associated muscles and bones [1,2,3]. To test the mechanical function of the plicidentine and venom groove during biting, we created a series of models where plicidentine infoldings and/or the venom groove were removed while keeping the total dentine volume approximately constant (electronic supplementary material, table S3). This was achieved by editing the 3D mesh file of the original F. leucobalia model using automated smoothing and mesh editing functions in 3-Matic v. High-resolution images of the histology sections of H. cyanocinctus and O. scutellatus were taken with a NanoZoomer 2.0HT digital slide scanner (Hamamatsu Photonics) at the Faculty of Health and Medical Sciences of the University of Adelaide and visualized in NDP view v. 2 (Hamamatsu Photonics)

Results

Discussion

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